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Special Focus: Mesenchymal Stem Cells – Review

Osteogenic Differentiation of Human Marrow-Derived Mesenchymal Stem Cells

Pierre J Marie1 Laboratory of Osteoblast Biology and PathologyUnité 606 INSERM, Hopital Lariboisière, 2 rue Ambroise Paré, 75475 Paris Cedex 10; and Université Paris, 7, France. +33 1 49 95 63 89; Fax: +33 1 49 95 84 52;[email protected]
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Olivia Fromigué1 Laboratory of Osteoblast Biology and PathologyUnité 606 INSERM, Hopital Lariboisière, 2 rue Ambroise Paré, 75475 Paris Cedex 10; and Université Paris, 7, France. +33 1 49 95 63 89; Fax: +33 1 49 95 84 52;[email protected]
Pages 539-548 | Published online: 18 Jul 2006

Bibliography

  • Owen M : Marrow stromal stem cells.J. Cell Sci. Suppl.10, 63–76 (1988).
  • Caplan AI : Mesenchymal stem cell.J. Orthop. Res.9(5), 641–650 (1991).
  • Prockop DJ : Marrow stromal cells as stem cells for nonhematopoietic tissues.Science276(5309), 71–74 (1997).
  • Bianco P , RobeyPG: Marrow stromal stem cells.J. Clin. Invest.105, 1663–1668 (2000).
  • Ahdjoudj S , FromiguéO, MariePJ: Plasticity and regulation of human bone marrow stromal osteoprogenitor cells: potential implication in the treatment of age-related bone loss.Histol. Histopathol.19(1), 151–157 (2004).
  • Friedenstein AJ : Precursor cells of mechanocytes.Int. Rev. Cytol.47, 327–359 (1976).
  • Ashton BA , AbdullahF, CaveJ et al.: Characterization of cells with high alkaline phosphatase activity derived from human bone and marrow: preliminary assessment of their osteogenicity. Bone6(5), 313–319 (1985).
  • Beresford JN : Osteogenic stem cells and the stromal system of bone and marrow.Clin. Orthop. Relat. Res. (240), 270–280 (1989).
  • Haynesworth SE , GoshimaJ, Goldberg VM, Caplan AI: Characterization of cells with osteogenic potential from human marrow. Bone13(1), 81–88 (1992).
  • Cheng SL , YangJW, RifasL, ZhangSF, AvioliLV: Differentiation of human bone marrow osteogenic stromal cells in vitro: induction of the osteoblast phenotype by dexamethasone.Endocrinology134(1), 277–286 (1994).
  • Rickard DJ , KassemM, HefferanTE, SarkarG, SpelsbergTC, RiggsBL: Isolation and characterization of osteoblast precursor cells from human bone marrow.J. Bone Miner. Res.11(3), 312–324 (1996).
  • Jaiswal N , HaynesworthSE, CaplanAI, BruderSP: Osteogenic differentiation of purified, culture-expanded human mesenchymal stem cells in vitro.J. Cell Biochem.64(2), 295–312 (1997).
  • Fromigué O , MariePJ, LomriA: Differential induction of the osteoblast phenotype by 1,25-dihydroxyvitamin D, dexamethasone and TGF-β2 in long-term cultures of human bone marrow stroma-derived osteoprogenitor cells.Cytokine9(8), 613–623 (1997).
  • Krebsbach PH , KuznetsovSA, BiancoP, RobeyPG: Bone marrow stromal cells: characterization and clinical application.Crit. Rev. Oral Biol. Med. 10(2), 165–81 (1999).
  • Herbertson A , AubinJE: Cell sorting enriches osteogenic populations in rat bone marrow stromal cell cultures.Bone21(6), 491–500 (1997).
  • Gronthos S , SimmonsPJ: The growth factor requirements of STRO-1-positive human bone marrow stromal precursors under serum-deprived conditions in vitro.Blood85, 929–940 (1995).
  • Oyajobi BO , LomriA, HottM, MariePJ: Isolation and characterization of human clonogenic osteoblast progenitors immunoselected from fetal bone marrow using STRO-1 monoclonal antibody.J. Bone Miner. Res.14(3), 351–361 (1999).
  • Stewart K , WalshS, ScreenJ et al.: Further characterization of cells expressing STRO-1 in cultures of adult human bone marrow stromal cells. J. Bone Miner. Res.14(8), 1345–1356 (1999).
  • Dennis JE , CarbilletJP, CaplanAI, CharbordP: The STRO-1+ marrow cell population is multipotential.Cells Tissues Organs170(2–3), 73–82 (2002).
  • Colter DC , SekiyaI, ProckopDJ: Identification of a subpopulation of rapidly self-renewing and multipotential adult stem cells in colonies of human marrow stromal cells.Proc. Natl Acad. Sci. USA98(14), 7841–7845 (2001).
  • Qi H , AguiarDJ, WilliamsSM, La Pean A, Pan W, Verfaillie CM: Identification of genes responsible for osteoblast differentiation from human mesodermal progenitor cells. Proc. Natl Acad. Sci. USA100(6), 3305–3310 (2003).
  • Hicok KC , ThomasT, GoriF, RickardDJ, SpelsbergTC, RiggsBL: Development and characterization of conditionally immortalized osteoblast precursor cell lines from human bone marrow stroma.J. Bone Miner. Res.13(2), 205–217 (1998).
  • Houghton A , OyajobiBO, FosterGA, RussellRG, StringerBM: Immortalization of human marrow stromal cells by retroviral transduction with a temperature sensitive oncogene: identification of bipotential precursor cells capable of directed differentiation to either an osteoblast or adipocyte phenotype.Bone22(1), 7–16 (1998).
  • Thomas T , GoriF, SpelsbergTC, KhoslaS, RiggsBL, ConoverCA: Response of bipotential human marrow stromal cells to insulin-like growth factors: effect on binding protein production, proliferation, and commitment to osteoblasts and adipocytes.Endocrinology140(11), 5036–5044 (1999)
  • Dennis JE , MerriamA, AwadallahA, Yoo JU, Johnstone B, Caplan AI: A quadripotential mesenchymal progenitor cell isolated from the marrow of an adult mouse. J. Bone Miner. Res.14(5), 700–709 (1999).
  • Pittenger MF , MackayAM, BeckSC et al.: Multilineage potential of adult human mesenchymal stem cells.Science284(5411), 143–147 (1999).
  • Ahdjoudj S , LasmolesF, OyajobiBO, LomriA, DelannoyP, MariePJ: Reciprocal control of osteoblast/chondroblast and osteoblast/adipocyte differentiation of multipotential clonal human marrow stromal F/STRO-1(+) cells.J. Cell Biochem.81(1), 23–38 (2000).
  • Muraglia A, Cancedda R, Quarto R: Clonal mesenchymal progenitors from human bone marrow differentiate in vitro according to a hierarchical model. J. Cell Sci.113(Pt 7), 1161–1166 (2000).
  • Beresford JN , BennettJH, DevlinC, Leboy PS, Owen ME: Evidence for an inverse relationship between the differentiation of adipocytic and osteogenic cells in rat marrow stromal cell cultures. J. Cell Sci.102, 341 (1992).
  • Nuttall ME, Patton AJ, Olivera DL, Nadeau DP, Gowen M: Human trabecular bone cells are able to express both osteoblastic and adipocytic phenotype: implications for osteopenic disorders. J. Bone Miner. Res.13(3), 371–382 (1998).
  • Park SR , OreffoRO, TriffittJT: Interconversion potential of cloned human marrow adipocytes in vitro.Bone24(6), 549–54 (1999).
  • Lecka-Czernik B , GubrijI, MoermanEJ et al.: Inhibition of Osf2/Cbfa1 expression and terminal osteoblast differentiation by PPAR γ2. J. Cell Biochem.74(3), 357–371 (1999).
  • Nuttall ME , GimbleJM: Controlling the balance between osteoblastogenesis and adipogenesis and the consequent therapeutic implications.Curr. Opin. Pharmacol.4(3), 290–294 (2004).
  • • Reviews the potential applications of mesenchymal stem cell (MSC) plasticity.
  • Leboy PS , BeresfordJN, DevlinC, Owen ME: Dexamethasone induction of osteoblast mRNAs in rat marrow stromal cell cultures. J. Cell Physiol. 146(3), 370–378 (1991).
  • Kamalia N , McCullochCA, TenebaumHC, LimebackH: Dexamethasone recruitment of self-renewing osteoprogenitor cells in chick bone marrow stromal cell cultures.Blood79(2), 320–326 (1992).
  • Malaval L , ModrowskiD, GuptaAK, Aubin JE: Cellular expression of bone-related proteins during in vitro osteogenesis in rat bone marrow stromal cell cultures. J. Cell Physiol.158(3), 555–572 (1994).
  • Benayahu D , KletterY, ZiporiD, WientroubS: Bone marrow-derived stromal cell line expressing osteoblastic phenotype in vitro and osteogenic capacity in vivo.J. Cell Physiol.140(1), 1–7 (1989).
  • Shui C , SpelsbergTC, RiggsBL, KhoslaS: Changes in Runx2/Cbfa1 expression and activity during osteoblastic differentiation of human bone marrow stromal cells.J. Bone Miner. Res.18(2), 213–221 (2003).
  • Marom R , ShurI, SolomonR, BenayahuD: Characterization of adhesion and differentiation markers of osteogenic marrow stromal cells.J. Cell Physiol. 202(1), 41–48 (2005).
  • Lian JB , JavedA, ZaidiSK et al.: Regulatory controls for osteoblast growth and differentiation: role of Runx/Cbfa/AML factors.Crit. Rev. Eukaryot. Gene Expr.14(1–2), 1–41(2004).
  • Fromigué O , MariePJ, LomriA: Bone morphogenetic protein-2 and transforming growth factor-β2 interact to modulate human bone marrow stromal cell proliferation and differentiation.J. Cell Biochem.68, 411–426 (1998).
  • Tamama K , FanVH, GriffithLG, BlairHC, WellsA: Epidermal growth factor as candidate for ex vivo expansion of bone marrow-derived mesenchymal stem cells.Stem Cells24(3), 686–695 (2005)
  • Kratchmarova I , BlagoevB, Haack-Sorensen M, Kassem M, Mann M: Mechanism of divergent growth factor effects in mesenchymal stem cell differentiation. Science308(5727), 1472–1477 (2005).
  • Luo Q , KangQ, SiW et al.: Connective tissue growth factor (CTGF) is regulated by Wnt and bone morphogenetic proteins signaling in osteoblast differentiation of mesenchymal stem cells. J. Biol. Chem.279(53), 55958–55968 (2004).
  • Kortesidis A , ZannettinoA, IsenmannS, ShiS, LapidotT, GronthosS: Stromal-derived factor-1 promotes the growth, survival, and development of human bone marrow stromal stem cells.Blood105(10), 3793–3801 (2005).
  • Martin I , MuragliaA, CampanileG, CanceddaR, QuartoR: Fibroblast growth factor-2 supports ex vivo expansion and maintenance of osteogenic precursors from human bone marrow.Endocrinology138(10), 4456–4462 (1997).
  • Pri-Chen S , PitaruS, LokiecF, SavionN: Basic fibroblast growth factor enhances the growth and expression of the osteogenic phenotype of dexamethasone-treated human bone marrow-derived bone-like cells in culture.Bone23(2), 111–117 (1998).
  • Kotev-Emeth S , PitaruS, Pri-ChenS, SavionN: Establishment of a rat long-term culture expressing the osteogenic phenotype: dependence on dexamethasone and FGF-2.Connect. Tissue Res. 43(4), 606–612 (2002).
  • Nishida S , YamaguchiA, TanizawaT et al.: Increased bone formation by intermittent parathyroid hormone administration is due to the stimulation of proliferation and differentiation of osteoprogenitor cells in bone marrow. Bone15(6), 717–723 (1994).
  • Kassem M , MosekildeL, EriksenEF: Growth hormone stimulates proliferation of normal human bone marrow stromal osteoblast precursor cells in vitro.Growth Regul. 4(3), 131–135 (1994).
  • Rickard DJ , KazhdanI, LeboyPS: Importance of 1,25-dihydroxyvitamin D3 and the nonadherent cells of marrow for osteoblast differentiation from rat marrow stromal cells.Bone16(6), 671–678 (1995).
  • Holzer G , EinhornTA, MajeskaRJ: Estrogen regulation of growth and alkaline phosphatase expression by cultured human bone marrow stromal cells.J. Orthop. Res. 20(2), 281–288 (2002).
  • Okazaki R, Inoue D, Shibata M et al.: Estrogen promotes early osteoblast differentiation and inhibits adipocyte differentiation in mouse bone marrow stromal cell lines that express estrogen receptor (ER) α or β. Endocrinology143(6), 2349–2356 (2002).
  • Thomas T , GoriF, KhoslaS, JensenMD, BurgueraB, RiggsBL: Leptin acts on human marrow stromal cells to enhance differentiation to osteoblasts and to inhibit differentiation to adipocytes. Endocrinology. 140(4), 1630–1638 (1999).
  • Scutt A , BertramP: Bone marrow cells are targets for the anabolic actions of prostaglandin E2 on bone: induction of a transition from nonadherent to adherent osteoblast precursors.J. Bone Miner. Res. 10(3), 474–487 (1995).
  • Spinella-Jaegle S , RawadiG, KawaiS et al.: Sonic hedgehog increases the commitment of pluripotent mesenchymal cells into the osteoblastic lineage and abolishes adipocytic differentiation. J. Cell Sci.114(Pt 11), 2085–2094 (2001).
  • Koch H , JadlowiecJA, CampbellPG: Insulin-like growth factor-I induces early osteoblast gene expression in human mesenchymal stem cells.Stem Cells Dev.14(6), 621–631 (2005).
  • Lecanda F , AvioliLV, ChengSL: Regulation of bone matrix protein expression and induction of differentiation of human osteoblasts and human bone marrow stromal cells by bone morphogenetic protein-2.J. Cell Biochem.67(3), 386–396 (1997).
  • Gori F, Thomas T, Hicok KC, Spelsberg TC, Riggs BL: Differentiation of human marrow stromal precursor cells: bone morphogenetic protein-2 increases OSF2/CBFA1, enhances osteoblast commitment, and inhibits late adipocyte maturation. J. Bone Miner. Res.14(9), 1522–1535 (1999).
  • Diefenderfer DL , OsyczkaAM, ReillyGC, LeboyPS: BMP responsiveness in human mesenchymal stem cells.Connect. Tissue Res.44(Suppl. 1), 305–311 (2003).
  • Friedman MS , LongMW, HankensonKD: Osteogenic differentiation of human mesenchymal stem cells is regulated by bone morphogenetic protein-6.J. Cell Biochem.98(3), 538–554 (2006).
  • Hanada K , DennisJE, CaplanAI: Stimulatory effects of basic fibroblast growth factor and bone morphogenetic protein-2 on osteogenic differentiation of rat bone marrow-derived mesenchymal stem cells.J. Bone Miner. Res.12(10), 1606–1614 (1997).
  • Beresford JN , JoynerCJ, DevlinC, Triffitt JT: The effects of dexamethasone and 1,25-dihydroxyvitamin D3 on osteogenic differentiation of human marrow stromal cells in vitro. Arch Oral Biol.39(11), 941–7 (1994).
  • Ogston N , HarrisonAJ, CheungHF, AshtonBA, HampsonG: Dexamethasone and retinoic acid differentially regulate growth and differentiation in an immortalised human clonal bone marrow stromal cell line with osteoblastic characteristics.Steroids67(11), 895–906 (2002).
  • Hong JH , HwangES, McManusMT et al.: TAZ, a transcriptional modulator of mesenchymal stem cell differentiation. Science. 12;309(5737), 1074–1078 (2005).
  • Kim YJ , KimHN, ParkEK et al.: The bone-related Zn finger transcription factor Osterix promotes proliferation of mesenchymal cells. Gene366, 145–151 (2006).
  • Tu Q , ValverdeP, ChenJ: Osterix enhances proliferation and osteogenic potential of bone marrow stromal cells.Biochem Biophys Res. Commun. 341(4), 1257–1265 (2006).
  • Celil AB , CampbellPG: BMP-2 and insulin-like growth factor-I mediate Osterix (Osx) expression in human mesenchymal stem cells via the MAPK and protein kinase D signaling pathways.J. Biol. Chem.280(36), 31353–31359 (2005).
  • Osyczka AM , LeboyPS: Bone morphogenetic protein regulation of early osteoblast genes in human marrow stromal cells is mediated by extracellular signal-regulated kinase and phosphatidylinositol 3-kinase signaling.Endocrinology146(8), 3428–3437 (2005).
  • Etheridge SL , SpencerGJ, HeathDJ, GeneverPG: Expression profiling and functional analysis of wnt signaling mechanisms in mesenchymal stem cells.Stem Cells22(5), 849–860 (2004).
  • • Reports the potential role of Wnt signaling in MSC differentiation.
  • Gaur T, Lengner CJ, Hovhannisyan H et al.: Canonical WNT signaling promotes osteogenesis by directly stimulating Runx2 gene expression. J. Biol. Chem.280(39), 33132–33140 (2005).
  • Bennett CN , LongoKA, WrightWS et al.: Regulation of osteoblastogenesis and bone mass by Wnt10b. Proc. Natl Acad. Sci. USA 102(9), 3324–3329 (2005).
  • de Boer J , SiddappaR, GasparC, van ApeldoornA, FoddeR, van BlitterswijkC: Wnt signaling inhibits osteogenic differentiation of human mesenchymal stem cells.Bone34(5), 818–826 (2004).
  • Boland GM , PerkinsG, HallDJ, Tuan RS: Wnt 3a promotes proliferation and suppresses osteogenic differentiation of adult human mesenchymal stem cells. J. Cell Biochem.93(6), 1210–1230 (2004).
  • Zhou S , EidK, GlowackiJ: Co-operation between TGF-β and Wnt pathways during chondrocyte and adipocyte differentiation of human marrow stromal cells.J. Bone Miner. Res. 19(3), 463–470 (2004).
  • Abdallah BM , JensenCH, GutierrezG, LeslieRG, JensenTG, KassemM: Regulation of human skeletal stem cells differentiation by Dlk1/Pref-1.J. Bone Miner. Res. 19(5), 841–852 (2004).
  • Gregory CA , PerryAS, ReyesE, ConleyA, GunnWG, ProckopDJ: Dkk-1-derived synthetic peptides and lithium chloride for the control and recovery of adult stem cells from bone marrow.J. Biol. Chem. 280(3), 2309–2323 (2005).
  • Moon RT , KohnAD, De Ferrari GV, Kaykas A: WNT and β-catenin signaling: diseases and therapies. Nature Rev. Genet.5(9), 691–701 (2004).
  • Pelled G , GT, AslanH, GazitZ, GazitD: Mesenchymal stem cells for bone gene therapy and tissue engineering.Curr. Pharm. Des.8(21), 1917–1928 (2002).
  • Tuan RS , BolandG, TuliR: Adult mesenchymal stem cells and cell-based tissue engineering.Arthritis Res. Ther.5(1), 32–45 (2003).
  • Derubeis AR , CanceddaR: Bone marrow stromal cells (BMSCs) in bone engineering: limitations and recent advances.Ann. Biomed. Eng.32(1), 160–165 (2004).
  • Kassem M : Mesenchymal stem cells: biological characteristics and potential clinical applications.Cloning Stem Cells6(4), 369–374 (2004).
  • Caplan AI : Mesenchymal stem cells: cell-based reconstructive therapy in orthopedics.Tissue Eng.11(7–8), 1198–1211 (2005).
  • Sotiropoulou PA , PerezSA, SalagianniM, BaxevanisCN, PapamichailM: Characterization of the optimal culture conditions for clinical scale production of human mesenchymal stem cells.Stem Cells24(5), 1409–1410 (2005).
  • Shahdadfar A , FronsdalK, HaugT, ReinholtFP, BrinchmannJE: In vitro expansion of human mesenchymal stem cells: choice of serum is a determinant of cell proliferation, differentiation, gene expression, and transcriptome stability.Stem Cells. 23(9), 1357–1366 (2005).
  • Petite H , ViateauV, BensaidW et al.: Tissue-engineered bone regeneration. Nat. Biotechnol.18(9), 959–963 (2000).
  • Kumar S , PonnazhaganS: Gene therapy for osteoinduction.Curr. Gene Ther.4(3), 287–296 (2004).
  • Simonsen JL , RosadaC, SerakinciN et al.: Telomerase expression extends the proliferative lifespan and maintains the osteogenic potential of human bone marrow stromal cells. Nature Biotechnol.20(6), 592–596 (2002).
  • Shi S , GronthosS, ChenS et al.: Bone formation by human postnatal bone marrow stromal stem cells is enhanced by telomerase expression. Nature Biotechnol.20(6), 587–591(2002).
  • Zhao Z , ZhaoM, XiaoG, FranceschiRT. Gene transfer of the Runx2 transcription factor enhances osteogenic activity of bone marrow stromal cells in vitro and in vivo. Mol. Ther.12(2), 247–253 (2005).
  • Kojima H , UemuraT: Strong and rapid induction of osteoblast differentiation by Cbfa1/Til-1 overexpression for bone regeneration.J. Biol. Chem.280(4), 2944–2953 (2005).
  • Turgeman G , PittmanDD, MullerR et al.: Engineered human mesenchymal stem cells: a novel platform for skeletal cell mediated gene therapy. J. Gene Med.3(3), 240–251(2001).
  • Foster LJ , ZeemannPA, LiC, MannM, JensenON, KassemM: Differential expression profiling of membrane proteins by quantitative proteomics in a human mesenchymal stem cell line undergoing osteoblast differentiation.Stem Cells23(9), 1367–1377 (2005).
  • Locklin RM , RiggsBL, HicokKC, Horton HF, Byrne MC, Khosla S: Assessment of gene regulation by bone morphogenetic protein 2 in human marrow stromal cells using gene array technology. J. Bone Miner. Res. 16(12), 2192–2204 (2001).
  • Silva WA Jr, Covas DT, Panepucci RA et al.: The profile of gene expression of human marrow mesenchymal stem cells. Stem Cells21(6), 661–669 (2003).
  • Yue B , LuB, DaiKR et al.: BMP2 gene therapy on the repair of bone defects of aged rats.Calcif. Tissue Int. 77(6), 395–403 (2005).
  • Tsuda H , WadaT, YamashitaT, HamadaH: Enhanced osteoinduction by mesenchymal stem cells transfected with a fiber-mutant adenoviral BMP2 gene.J. Gene Med.7(10), 1322–1334 (2005).
  • Van Damme A , ThorrezL, MaL et al.: Efficient lentiviral transduction and improved engraftment of human bone marrow mesenchymal cells. Stem Cells24(4), 896–907(2005).
  • Franceschi RT : Biological approaches to bone regeneration by gene therapy.J. Dent. Res.84(12),1093–103 (2005.
  • • A recent review on the current gene therapy approaches for bone regeneration.
  • Kofron MD , LiX, LaurencinCT: Protein- and gene-based tissue engineering in bone repair.Curr. Opin. Biotechnol.15(5), 399–405 (2004).

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